Primates, Atelidae): Interactions and the Development of Behavioral Patterns 1
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The first seven months of an infant of Alouatta guariba (Humboldt) (Primates, Atelidae): interactions and the development of behavioral patterns 1 João M. D. Miranda 2, Lucas M. Aguiar 2, Gabriela Ludwig 2, Rodrigo F. Moro-Rios 2, 3 & Fernando C. Passos 2 1 Contribution number 1564 of the Departamento de Zoologia, Universidade Federal do Paraná. 2 Laboratório de Biodiversidade, Conservação e Ecologia de Animais Silvestres, Departamento de Zoologia, Universidade Federal do Paraná. Caixa Postal 19020, 81531-980 Curitiba, Paraná, Brasil. E-mail: [email protected]; [email protected]; [email protected]; [email protected]; [email protected]. 3 Bolsista CNPq/PIBIC. ABSTRACT. The development of the interactions of an infant primate with its mother and the other members of its social group plays a special role in the ethology and demography of the species, with consequences for their survive and their conservation. The objective of the present study is to investigate the development of an infant of Alouatta guariba (Humboldt, 1812) in the wild, its behavior and interactions during its first seven months of age, in a remnant of Araucaria Pine Forest in Paraná State, Brazil. Using the method of instantaneous scanning with 5 min intervals, a total of 46 hours and 15 minutes of direct observation (555 individual records) showed that the infant behavioral patterns during its first four months were characterized by high dependency, which decreased progressively until the appearance of typically juvenile behaviors during the remaining 3 months. The first records of feeding on solid food, tail functionality and allomaternal care were also recorded and discussed. This work contributes to an understanding of the ontogenetic development of a poorly known aspect of this species, and thus for a more understanding of the genus Alouatta Lacépède, 1799. KEY WORDS. Infancy, ontogenetic development, parental care, social behavior. RESUMO. Os sete primeiros meses de um infante de Alouatta guariba (Humboldt) (Primatesimates, Atelidae)Atelidae): interações e desenvolvimento dos padrões comportamentais. O desenvolvimento das interações do infante primata com a mãe e demais membros do grupo social tem importância na etologia e na demografia da espécie, apresentando profundas conseqüências para sua sobrevivência e portanto, na conservação da espécie. O objetivo deste trabalho foi estudar o desenvolvimento de um infante de Alouatta guariba (Humboldt, 1812) em vida livre, seu comportamento e interações durante os sete primeiros meses de vida, em um remanescente de Floresta Ombrófila Mista, Estado do Paraná, Brasil. Através do método de varredura instantânea com intervalo de cinco minutos, um total de 46 horas e 15 minutos de observações diretas (555 registros individuais) mostraram que os padrões comportamentais do infante foram de alta dependência nos primeiros quatro meses, diminuindo progressivamente até o aparecimento dos comportamentos típicos de indivíduos juvenis durante os últimos três meses. Os primeiros registros de alimen- tação sólida, funcionalidade da cauda e registros de cuidados alomaternais também foram tomados e discutidos, contribuindo para o entendimento do desenvolvimento deste infante. PALAVRAS CHAVE. Comportamento social, cuidado parental, desenvolvimento ontogenético, infância. The principal, longest and most intense social link among pri- ing and interacting with her, the infant learns what to eat and mates is that between mother and offspring (FEDIGAN 1982, STRIER what to fear, who to dominate and who to submit to, where to 2003). Contrary to other mammal orders, the survivorship of walk, sleep and drink (FEDIGAN 1982). In addition, the mother the infant primate is completely dependent on the care pro- might represent a source of thermoregulation, grooming and vided by members of its social group, particularly through defense against predators and other aggressors (STRIER 2003). maternal care. Therefore, it is crucial that mothers recognize Over time, the infant progressively becomes independent of their infants as their own offspring, and that they are moti- her, acquiring important biological and psychological advan- vated to provide maternal care (MAESTRIPIERI 2001). By observ- tages, such as the familiarity with its physical and social mi- Revista Brasileira de Zoologia 22 (4): 1191–1195, dezembro 2005 1192 J. M. D. Miranda et al. lieu. At the same time, this enables the mother additional The goal of the present study was to investigate the de- chances for mating and reproducing, providing simultaneous velopment of an infant of Alouatta guariba, subspecies A. g. increase in several facets of her inclusive fitness (RHEINGOLD & clamitans Cabrera, 1940 in the wild, as well as its maternal and ECKERMAN 1970). allomaternal relationships during the first seven months of its Starting with the pioneer work of HARLOW & ZIMMERMANN life, in a remnant of Araucaria Pine forest in Southern Brazil. (1959) on the affective links of infants of Macaca Lacépède, 1799, several studies in the field and in captivity, have addressed MATERIAL AND METHODS the behavioral interactions between mother and offspring in The present study was conducted in a 700 ha remnant of non–human primates, both in the Old and in the New World Araucaria Pine Forest located in the Bugre district, Municipal- (RHEINGOLD & ECKERMAN 1970). Therefore, special emphasis on ity of Balsa Nova, State of Paraná (25º29’52”W and 49º39’24”S). the study of this behavior are of crucial importance to under- The climate in the region is of the Cfb type according to the stand the biology, ethology and demography of these animals, Köpen classification (IAPAR 1978), with an average annual tem- given that, once the success of this ontogenetic phase is guar- perature of 18ºC and average annual rainfall of 1600 mm (data anteed, there is increased chance of recruitment and thus of obtained from the Meteorological Station of the Municipality group and population growth. of Lapa). Being composed mostly of altered primary forest, this In addition to maternal care, paternal investments and remnant experienced a pressure of selective tree cutting over other forms of allomaternal care might be present in several spe- its history. Currently, this region is conserved as part of the cies depending on their social systems. The quality and quan- State Area of Environmental Protection of the Devonian Scarp. tity of allomaternal interactions with infants would depend on This study was planned during the monitoring of one of the degree of kinship: when group members are closely related the groups of A. guariba that have been followed in the study (1), the interactions of this kind could be more cooperative; area since 2002 (MIRANDA & PASSOS 2004, 2005). Beginning on however, when group members are not closely related (2), ex- the birth of the infant in question (in the week between 11 pected interactions could be of a more competitive nature (CLARKE and 18 April 2004), it was possible to study its development et al. 1998). and its interactions in the wild. In April of 2004, time of the In the case of neotropical primates, polygynic systems birth of the infant, the group was composed by an adult male, such as the one found in Cebus Erxleben, 1777 and monogamic two adult females, a sub-adult male, a juvenile I and a juvenile families such as those found in callitrichids might produce the II (age/sex classification sensu MENDES 1989). During the next allomaternal interactions expected under (1) (see SÁNCHEZ et al. seven months, this infant and its mother were the main foci of 1999, SCHRADIN & ANZENBERGER 2001, TARDIFF et al. 2002). On the observation, being followed during data collection with respect other hand, in the genus Alouatta Lacépède, 1799 the social to their interactions and behavioral patterns. These data were system is shaped by male and female migrations, generating obtained using the method of instantaneous scann sampling lower relatedness, causing interactions to be expected to corre- with records every five minutes (ALTMANN 1974). spond to (2). However, few studies have addressed directly those The infant was born in the Fall of 2004, more precisely interactions in species of the genus Alouatta. In general, such in the week between 11 and 18 of April, when it was first seen descriptions are concentrated on the two most studied species: and, together with its mother and the other members of the A. seniculus (Linnaeus, 1766) and A. palliata (Gray, 1848) (LYALL group, started to be followed by the observers. The mother and 1996 and see reviews in NEVILLE et al. 1988, DEFLER 2004), in the infant were followed during the first seven months of the addition to the works by CALEGARO-MARQUES & BICCA-MARQUES infant’s life, totaling 46 hours and 15 minutes of direct obser- (1993a) on Alouatta caraya (Humboldt, 1812). vations, and 555 individual records. With regard to the investigation of infancy of individu- als of A. guariba (Humboldt, 1812), a species endemic to the RESULTS South and Southeast portions of the Brazilian Atlantic Rainforest, no study has hitherto given priority to this theme During the first days of its life, the infant was positioned in such studies. Given that it is still unclear how the informa- 100% of the time ventrally of its mother, being active only tion based on the three well known species described above during nursing (Fig. 1). At the end of the first month of life, can be extrapolated to the rest of the genus Alouatta (RUMIZ the use of this position gradually started to decrease and the 1990), studies on the behavioral mother-offspring interaction dorsum of the mother was used more frequently: 60 % in the in A. guariba and other species are necessary to understand this ventral position and 30% in the dorsal position. Also follow- genus in a more holistic way. This information might also con- ing a progressive manner, peaking during its fifth month of tribute vital information for the conservation of this species, age, the infant began to behave more independently, with ex- which is currently enlisted vulnerable to extinction in several ploratory behaviors and movements away from its mother (Fig.